Abstract
Salinity tolerance is critical during the early ontogeny of amphibians, shaping future population size, health and dispersal in a certain area. We focused our research on two related anurans with similar ecological niches—Pelobates fuscus and P. syriacus—inhabiting the western Black Sea coast, at the limits of their ranges. We hypothesize that their differences in salinity tolerance are shaping the actual range limits in coastal areas, within the sympatry zone. We quantified experimentally the impact of salinity (range 0–9‰) during early ontogeny to ask if salinity can modulate their coexistence, by affecting differently reproductive success and fitness. Exposure to salinity from egg to developmental stage Gosner 25 caused mild to severe malformations and affected survival and size in both species, but the impact was lower in P. syriacus compared to P. fuscus when exposed to salt concentrations of 6‰. Embryos of either species did not survive the 9‰ salinity concentration. We expect that increases in salinization up to 6‰ could severely reduce the range of P. fuscus, but not P. syriacus, in coastal areas. These results are highly relevant for the conservation of P. fuscus, which is already declining across Europe.
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Agasyan, A., A. Avci, B. Tuniyev, J. Crnobrnja Isailovic, P. Lymberakis, C. Andrén, D. Cogălniceanu, J. Wilkinson, N. Ananjeva, N. Üzüm, N. Orlov, R. Podloucky, S. Tuniyev & K. Uğur, 2009. Pelobates fuscus. The IUCN Red List of Threatened Species: e.T16498A5951455. http://dx.doi.org/10.2305/IUCN.UK.2009.RLTS.T16498A5951455.en.
Alexander, L. G., S. P. Lailvaux, J. H. Pechmann & P. J. DeVries, 2012. Effects of salinity on early life stages of the Gulf Coast toad, Incilius nebulifer (Anura: Bufonidae). Copeia 2012: 106–114.
Altwegg, R. & H. U. Reyer, 2003. Patterns of natural selection on size at metamorphosis in water frogs. Evolution 57: 872–882.
Araújo, M. B., W. Thuiller & R. G. Pearson, 2006. Climate warming and the decline of amphibians and reptiles in Europe. Journal of Biogeography 33: 1712–1728.
Baillie, J. E. M., J. Griffiths, S. T. Turvey, J. Loh & B. Collen, 2010. Evolution Lost: Status and Trends of the World’s Vertebrates. Zoological Society of London, London.
Beebee, T. J. C., 1985. Salt tolerances of natterjack toad (Bufo calamita) eggs and larvae from coastal and inland populations in Britain. Herpetological Journal 1: 14–16.
Bernabò, I., A. Bonacci, F. Coscarelli, M. Tripepi & E. Brunelli, 2013. Effects of salinity stress on Bufo balearicus and Bufo bufo tadpoles: tolerance, morphological gill alterations and Na+/K+-ATPase localization. Aquatic Toxicology 132: 119–133.
Berven, K. A., 1990. Factors affecting population fluctuations in larval and adult stages of the wood frog (Rana sylvatica). Ecology 71: 1599–1608.
Blaustein, A. R., S. C. Walls, B. A. Bancroft, J. J. Lawler, C. L. Searle & S. S. Gervasi, 2010. Direct and indirect effects of climate change on amphibian populations. Diversity 2: 281–313.
Boutilier, R. G., D. F. Stiffler & D. P. Toews, 1992. Exchange of respiratory gases, ions and water in amphibious and aquatic amphibians. In Feder, M. E. & W. W. Burggren (eds), Environmental Physiology of the Amphibians. University of Chicago Press, Chicago: 81–124.
Brown, M. E. & S. C. Walls, 2013. Variation in salinity tolerance among larval anurans: implications for community composition and the spread of an invasive, non-native species. Copeia 2013: 543–551.
Burraco, P. & I. Gómez-Mestre, 2016. Physiological stress responses in amphibian larvae to multiple stressors reveal marked anthropogenic effects even below lethal levels. Physiological and Biochemical Zoology 89: 462–472.
Cañedo-Argüelles, M., C. P. Hawkins, B. J. Kefford, R. B. Schäfer, B. J. Dyack, S. Brucet, D. Buchwalter, J. Dunlop, O. Frör, J. Lazorchak, E. Coring, H. R. Fernandez, W. Goodfellow, A. L. G. González Achem, S. Hatfield-Dodds, B. K. Karimov, P. Mensah, J. R. Olson, C. Piscart, N. Prat, S. Ponsá, C. J. Schulz & A. J. Timpano, 2016. Saving freshwater from salts. Science 351: 914–916.
Church, J. A., P. U. Clark, A. Cazenave, J. M. Gregory, S. Jevrejeva, A. Levermann, M. A. Merrifield, G. A. Milne, R. S. Nerem, P. D. Nunn, A. J. Payne, W. T. Pfeffer, D. Stammer & A. S. Unnikrishnan, 2013. Sea level change. In Stocker, T. F., D. Qin, G. -K. Plattner, M. Tignor, S. K. Allen, J. Boschung, A. Nauels, Y. Xia, V. Bex & P. M. Midgley (eds), Climate Change 2013: The Physical Science Basis. Working Group I Contribution to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge: 1137–1216.
Cogălniceanu, D., F. Aioanei & B. Matei, 2000. Amfibienii din România. Determinator. Ars Docendi, Bucharest.
Cogălniceanu, D., P. J. Székely, C. Samoilă, R. Iosif, M. Tudor, R. Plăiaşu, F. Stănescu & L. Rozylowicz, 2013. Diversity and distribution of amphibians in Romania. ZooKeys 296: 35–57.
Collins, S. J. & R. W. Russell, 2009. Toxicity of road salt to Nova Scotia amphibians. Environmental Pollution 157: 320–324.
Craft, C., J. Clough, J. Ehman, S. Joye, R. Park, S. Pennings, H. Guo & M. Machmuller, 2008. Forecasting the effects of accelerated sea-level rise on tidal marsh ecosystem services. Frontiers in Ecology and the Environment 7: 73–78.
Crump, M. L., 1991. Choice of oviposition site and egg load assessment by a treefrog. Herpetologica 47: 308–315.
Degani, G. & E. Nevo, 1986. Osmotic stress and osmoregulation of tadpoles and juveniles of Pelobates syriacus. Comparative Biochemistry and Physiology Part A 83: 365–370.
Denoël, M., M. Bichot, G. F. Ficetola, J. Delcourt, M. Ylieff, P. Kestemont & P. Poncin, 2010. Cumulative effects of road de-icing salt on amphibian behavior. Aquatic Toxicology 99: 275–280.
de Oliveira, I., D. Rödder & L. F. Toledo, 2016. Potential worldwide impacts of sea level rise on coastal-lowland anurans. North-Western Journal of Zoology 12: 91–101.
Džukić, G., V. Beškov, V. Sidorovska, D. Cogălniceanu & M. Kalezić, 2008. Contemporary chorology of the spadefoot toads (Pelobates spp.) in the Balkan Peninsula. Zeitschrift für Feldherpetologie 15: 61–78.
Eggert, C., D. Cogălniceanu, M. Veith, G. Dzukic & P. Taberlet, 2006. The declining Spadefoot toad, Pelobates fuscus (Pelobatidae): paleo and recent environmental changes as a major influence on current population structure and status. Conservation Genetics 7: 185–195.
El Hamoumi, R., M. Dakki & M. Thevenot, 2007. Etude écologique des larves d’anoures du Maroc. Bulletin de l’Institut Scientifique, Rabat 29: 27–34.
Erwin, K. L., 2009. Wetlands and global climate change: the role of wetland restoration in a changing world. Wetlands Ecology and Management 17: 71–84.
Escoriza, D., 2013. New data on larval development in Pelobates varaldii. The Herpetological Bulletin 125: 10–13.
European Union (EU), 1992. Council directive 92/43/EEC of 21 May 1992 on the conservation of natural habitats and of wild fauna and flora. Official Journal L 206: 7–50.
Findlay, S. E. & V. R. Kelly, 2011. Emerging indirect and long-term road salt effects on ecosystems. Annals of the New York Academy of Sciences 1223: 58–68.
Gómez-Mestre, I. & M. Tejedo, 2002. Geographic variation in asymmetric competition: a case study with two larval anuran species. Ecology 83: 2102–2111.
Gómez-Mestre, I. & M. Tejedo, 2003. Local adaptation of an anuran amphibian to osmotically stressful environments. Evolution 57: 1889–1899.
Gómez-Mestre, I. & M. Tejedo, 2004. Contrasting patterns of quantitative and neutral genetic variation in locally adapted populations of the natterjack toad, Bufo calamita. Evolution 58: 2343–2352.
Gómez-Mestre, I., M. Tejedo, E. Ramayo & J. Estepa, 2004. Developmental alterations and osmoregulatory physiology of a larval anuran under osmotic stress. Physiological and Biochemical Zoology 77: 267–274.
Gordon, M. S. & V. A. Tucker, 1965. Osmotic regulation in the tadpoles of the crab-eating frog (Rana cancrivora). Journal of Experimental Biology 42: 437–445.
Gosner, K. L., 1960. A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16: 183–190.
Grinevetsky, S. R., I. S. Zonn, S. S. Zhiltsov, A. N. Kosarev & A. G. Kostianoy, 2015. The Black Sea Encyclopedia. Springer, Berlin.
Halse, S. A., J. K. Ruprecht & A. M. Pinder, 2003. Salinisation and prospects for biodiversity in rivers and wetlands of south-west Western Australia. Australian Journal of Botany 51: 673–688.
Haramura, T., 2008. Experimental test of spawning site selection by Buergeria japonica (Anura: Rhacophoridae) in response to salinity level. Copeia 2008: 64–67.
Haramura, T., 2011. Use of oviposition sites by a rhacophorid frog inhabiting a coastal area in Japan. Journal of Herpetology 45: 432–437.
Hart, B. T., P. S. Lake, J. A. Webb & M. R. Grace, 2003. Ecological risk to aquatic systems from salinity increases. Australian Journal of Botany 51: 689–702.
Herbert, E. R., P. Boon, A. J. Burgin, S. C. Neubauer, R. B. Franklin, M. Ardón, K. N. Hopfensperger, L. P. M. Lamers & P. Gell, 2015. A global perspective on wetland salinization: ecological consequences of a growing threat to freshwater wetlands. Ecosphere 6: 1–43.
Hof, C., M. B. Araújo, W. Jetz & C. Rahbek, 2011. Additive threats from pathogens, climate and land-use change for global amphibian diversity. Nature 480: 516–519.
Hopkins, G. R. & E. D. Brodie Jr., 2015. Occurrence of amphibians in saline habitats: a review and evolutionary perspective. Herpetological Monographs 29: 1–27.
Iosif, R., M. Papeş, C. Samoilă & D. Cogălniceanu, 2014. Climate-induced shifts in the niche similarity of two related spadefoot toads (genus Pelobates). Organisms Diversity & Evolution 14: 397–408.
Jara, F. G. & M. G. Perotti, 2010. Risk of predation and behavioural response in three anuran species: influence of tadpole size and predator type. Hydrobiologia 644: 313–324.
Johnson, P. T. J., M. K. Reeves, S. K. Krest & A. E. Pinkney, 2010. A decade of deformities: advances in our understanding of amphibian malformations and their implications. In Sparling, D. W., G. Linder, C. A. Bishop & S. K. Krest (eds), Ecotoxicology of Amphibians and Reptiles, 2nd ed. Society of Environmental Toxicology and Chemistry Press, Pensacola: 511–536.
Junk, W. J., S. An, C. M. Finlayson, B. Gopal, J. Květ, S. A. Mitchell, W. J. Mitsch & R. D. Robarts, 2013. Current state of knowledge regarding the world’s wetlands and their future under global climate change: a synthesis. Aquatic Sciences 75: 151–167.
Karraker, N. E., 2007. Are embryonic and larval green frogs (Rana clamitans) insensitive to road deicing salt? Herpetological Conservation and Biology 2: 35–41.
Karraker, N. E., J. P. Gibbs & J. R. Vonesh, 2008. Impacts of road deicing salt on the demography of vernal pool-breeding amphibians. Ecological Applications 18: 724–734.
Karraker, N. E., J. Arrigoni & D. Dudgeon, 2010. Effects of increased salinity and an introduced predator on lowland amphibians in Southern China: species identity matters. Biological Conservation 143: 1079–1086.
Kaushal, S. S., P. M. Groffman, G. E. Likens, K. T. Belt, W. P. Stack, V. R. Kelly, L. E. Band & G. T. Fisher, 2005. Increased salinization of fresh water in the northeastern United States. Proceedings of the National Academy of Sciences of the United States of America 102: 13517–13520.
Kearney, B. D., P. G. Byrne & R. D. Reina, 2016. Short-and long-term consequences of developmental saline stress: impacts on anuran respiration and behaviour. Royal Society Open Science 3: 150640.
Metcalfe, N. B. & P. Monaghan, 2001. Compensation for a bad start: grow now, pay later? Trends in Ecology & Evolution 16: 254–260.
Morey, S. & D. Reznick, 2001. Effects of larval density on postmetamorphic spadefoot toads (Spea hammondii). Ecology 82: 510–522.
Munwes, I., E. Geffen, U. Roll, A. Friedmann, A. Daya, Y. Tikochinski & S. Gafny, 2010. The change in genetic diversity down the core-edge gradient in the eastern spadefoot toad (Pelobates syriacus). Molecular Ecology 19: 2675–2689.
Nicholls, R. J., F. M. Hoozemans & M. Marchand, 1999. Increasing flood risk and wetland losses due to global sea-level rise: regional and global analyses. Global Environmental Change 9: S69–S87.
Nyström, P., L. Birkedal, C. Dahlberg & C. Brönmark, 2002. The declining spadefoot toad Pelobates fuscus: calling site choice and conservation. Ecography 25: 488–498.
Osland, M. J., N. M. Enwright, R. H. Day, C. A. Gabler, C. L. Stagg & J. B. Grace, 2016. Beyond just sea-level rise: considering macroclimatic drivers within coastal wetland vulnerability assessments to climate change. Global Change Biology 22: 1–11.
Oude Essink, G. H. P., E. S. Van Baaren & P. G. De Louw, 2010. Effects of climate change on coastal groundwater systems: a modeling study in the Netherlands. Water Resources Research 46: W00F04.
Richards, S. J. & C. M. Bull, 1990. Size-limited predation on tadpoles of three Australian frogs. Copeia 1990: 1041–1046.
Sanzo, D. & S. J. Hecnar, 2006. Effects of road de-icing salt (NaCl) on larval wood frogs (Rana sylvatica). Environmental Pollution 140: 247–256.
Shpun, S., J. Hoffman, E. Nevo & U. Katz, 1993. Is the distribution of Pelobates syriacus related to its limited osmoregulatory capacity? Comparative Biochemistry and Physiology Part A 105: 135–139.
Sidorovska, V., K. Ljubisavljevic, G. Dzukic & M. L. Kalezic, 2002. Tadpole morphology of two spadefoot toads (Pelobates fuscus and P. syriacus) (Amphibia, Anura, Pelobatidae). Spixiana 25: 183–191.
Smith, M. J., E. S. G. Schreiber, M. P. Scroggie, M. Kohout, K. Ough, J. Potts, R. Lennie, D. Turnbull, C. Jin & T. I. M. Clancy, 2007. Associations between anuran tadpoles and salinity in a landscape mosaic of wetlands impacted by secondary salinisation. Freshwater Biology 52: 75–84.
Sridhar, V. V. & D. Bickford, 2015. Oviposition site selection in the Malayan Giant Frog (Limnonectes blythii) in Singapore: conservation implications. Asian Herpetological Research 6: 184–188.
Stanev, E. V. & E. L. Peneva, 2001. Regional sea level response to global climatic change: Black Sea examples. Global and Planetary Change 32: 33–47.
Stănescu, F., R. Iosif, D. Székely, P. Székely, D. Roşioru & D. Cogălniceanu, 2013. Salinity tolerance in Pelobates fuscus (Laurenti, 1768) tadpoles (Amphibia: Pelobatidae). Travaux du Muséum National d’Histoire Naturelle” Grigore Antipa 56: 103–108.
Stănescu, F., R. Iosif, P. Székely, D. Székely & D. Cogălniceanu, 2016. Mass migration of Pelobates syriacus (Boettger, 1889) metamorphs. Herpetozoa 29: 87–89.
Stewart, K., S. Kassakian, M. Krynytzky, D. DiJulio & J. W. Murray, 2007. Oxic, suboxic, and anoxic conditions in the Black Sea. In Yanko-Hombach, V., A. S. Gilbert, N. Panin & P. M. Dolukhanov (eds), The Black Sea Flood Question: Changes in Coastline, Climate, and Human Settlement. Springer, Dordrecht: 1–21.
Stuart, S. N., J. S. Chanson, N. A. Cox, B. E. Young, A. S. Rodrigues, D. L. Fischman & R. W. Waller, 2004. Status and trends of amphibian declines and extinctions worldwide. Science 306: 1783–1786.
Takahashi, M., 2007. Oviposition site selection: pesticide avoidance by gray treefrogs. Environmental Toxicology and Chemistry 26: 1476–1480.
Tarkhnishvili, D., I. Serbinova & A. Gavashelishvili, 2009. Modelling the range of Syrian spadefoot toad (Pelobates syriacus) with combination of GIS-based approaches. Amphibia-Reptilia 30: 401–412.
Tarvin, R. D., C. S. Bermudez, V. S. Briggs & K. M. Warkentin, 2015. Carry-over effects of size at metamorphosis in red-eyed treefrogs: higher survival but slower growth of larger metamorphs. Biotropica 47: 218–226.
Thirion, J. M., 2014. Salinity of the reproduction habitats of the Western spadefoot toad Pelobates cultripes (Cuvier, 1829), along the Atlantic coast of France. Herpetozoa 27: 13–20.
Tsimplis, M. N., S. A. Josey, M. Rixen & E. V. Stanev, 2004. On the forcing of sea level in the Black Sea. Journal of Geophysical Research: Oceans 109(C8): 3237–3249.
Uchiyama, M. & H. Yoshizawa, 1992. Salinity tolerance and structure of external and internal gills in tadpoles of the crab-eating frog, Rana cancrivora. Cell and Tissue Research 267: 35–44.
Viertel, B., 1999. Salt tolerance of Rana temporaria: spawning site selection and survival during embryonic development (Amphibia, Anura). Amphibia-Reptilia 20: 161–171.
Williams, W. D., 1999. Salinisation: a major threat to water resources in the arid and semi-arid regions of the world. Lakes & Reservoirs: Research & Management 4: 85–91.
Williams, W. D., 2001. Anthropogenic salinisation of inland waters. Hydrobiologia 466: 329–337.
Wu, C. S., I. Gómez-Mestre & Y. C. Kam, 2012. Irreversibility of a bad start: early exposure to osmotic stress limits growth and adaptive developmental plasticity. Oecologia 169: 15–22.
Acknowledgements
The Romanian National Authority for Scientific Research CNCS–UEFISCDI supported our research through Grant PN-II-ID-PCE-2011-3-0173. We are grateful to Danube Delta Biosphere Reserve Administration and the Ethics Committee from Ovidius University of Constanta for providing all the necessary permits and supporting our research in the study area. We thank our colleagues Elena Buhaciuc, Iosif Ruben and Monica Bogdan for help during fieldwork. We are grateful to our reviewers for their constructive comments and recommendations.
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Stănescu, F., Székely, D., Székely, P. et al. The impact of salinity on early developmental stages in two sympatric spadefoot toads and implications for amphibian conservation in coastal areas. Hydrobiologia 792, 357–366 (2017). https://doi.org/10.1007/s10750-016-3074-2
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DOI: https://doi.org/10.1007/s10750-016-3074-2